Discrimination between Closely Related Cellular Metabolites by the SAM-I Riboswitch

Journal of Molecular Biology

Volumn 396, Issue 3, 2010, Pages 761-772

  Montange, Rebecca K ^a   Mondragón, Estefanía ^a   van Tyne, Daria ^a   Garst, Andrew D ^a   Ceres, Pablo ^a   Batey, R T ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Isothermal titration calorimetry; Non protein coding RNA; Riboregulation; S adenosylmethionine; X ray crystallography

Indexed keywords

S ADENOSYLHOMOCYSTEINE; S ADENOSYLMETHIONINE; SINEFUNGIN; SULFONIUM DERIVATIVE; ADENOSINE; BACTERIAL RNA; DRUG DERIVATIVE; MESSENGER RNA;

ARTICLE; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ELECTRICITY; ISOTHERMAL TITRATION CALORIMETRY; METABOLITE; PRIORITY JOURNAL; PROTEIN DOMAIN; RIBOSWITCH; RNA SEQUENCE; STATIC ELECTRICITY; X RAY; BASE PAIRING; CHEMISTRY; CONFORMATION; GENETICS; KINETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS);

ADENOSINE; BASE PAIRING; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; KINETICS; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; RNA, BACTERIAL; RNA, MESSENGER; S-ADENOSYLHOMOCYSTEINE; S-ADENOSYLMETHIONINE;

EID: 77949327506     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.12.007     Document Type: Article

References (54)

1. Winkler W.C. Riboswitches and the role of noncoding RNAs in bacterial metabolic control. Curr. Opin. Chem. Biol. 2005, 9:594-602.
2. Wang J.X., Breaker R.R. Riboswitches that sense S-adenosylmethionine and S-adenosylhomocysteine. Biochem. Cell Biol. 2008, 86:157-168.
3. Epshtein V., Mironov A.S., Nudler E. The riboswitch-mediated control of sulfur metabolism in bacteria. Proc. Natl Acad. Sci. USA 2003, 100:5052-5056.
4. McDaniel B.A., Grundy F.J., Artsimovitch I., Henkin T.M. Transcription termination control of the S box system: direct measurement of S-adenosylmethionine by the leader RNA. Proc. Natl Acad. Sci. USA 2003, 100:3083-3088.
5. Winkler W.C., Nahvi A., Sudarsan N., Barrick J.E., Breaker R.R. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat. Struct. Biol. 2003, 10:701-707.
6. Corbino K.A., Barrick J.E., Lim J., Welz R., Tucker B.J., Puskarz I. Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria. Genome Biol. 2005, 6:R70.
7. Fuchs R.T., Grundy F.J., Henkin T.M. The S(MK) box is a new SAM-binding RNA for translational regulation of SAM synthetase. Nat. Struct. Mol. Biol. 2006, 13:226-233.
8. Weinberg Z., Regulski E.E., Hammond M.C., Barrick J.E., Yao Z., Ruzzo W.L., Breaker R.R. The aptamer core of SAM-IV riboswitches mimics the ligand-binding site of SAM-I riboswitches. RNA 2008, 14:822-828.
9. Montange R.K., Batey R.T. Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 2006, 441:1172-1175.
10. Lu C., Smith A.M., Fuch R.T., Ding F., Rajashankar K., Henkin T.M., Ke A. Crystal structure of the SAM-III/SAM(MK) riboswitch reveal the SAM-dependent translation inhibition mechanism. Nat. Struct. Mol. Biol. 2008, 15:1076-1083.
11. Gilbert S.D., Rambo R.P., VanTyne D., Batey R.T. Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat. Struct. Mol. Biol. 2008, 15:177-182.
12. Ueland P.M. Pharmacological and biochemical aspects of S-adenosylhomocysteine and S-adenosylhomoecysteine hydrolase. Pharmacol. Rev. 1982, 34:223-253.
13. Lim J., Winkler W.C., Nakamura S., Scott V., Breaker R.R. Molecular-recognition characteristics of SAM-binding riboswitches. Angew. Chem., Int. Ed. Engl. 2006, 45:964-968.
14. Blount K.F., Breaker R.R. Riboswitches as antibacterial drug targets. Nat. Biotechnol. 2006, 24:1558-1564.
15. Barrick J.E., Breaker R.R. The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol. 2007, 8:R239.
16. Gilbert S.D., Montange R.K., Stoddard C.D., Batey R.T. Structural studies of the purine and SAM binding riboswitches. Cold Spring Harbor Symp. Quant. Biol. 2006, 71:259-268.
17. Derewenda Z.S., Vekilov P.G. Entropy and surface engineering in protein crystallization. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2006, 62:116-124.
18. Yamada H., Tamada T., Kosaka M., Miyata K., Fujiki S., Tano M. 'Crystal lattice engineering,' an approach to engineer protein crystal contacts by creating intermolecular symmetry: crystallization and structure determination of a mutant human RNase 1 with a hydrophobic interface of leucines. Protein Sci. 2007, 16:1389-1397.
19. Bauman J.D., Das K., Ho W.C., Baweja M., Himmel D.M., Clark A.D.J. Crystal engineering of HIV-1 reverse transcriptase for structure-based drug design. Nucleic Acids Res. 2008, 36:5083-5092.
20. MacElrevey C., Spitale R.C., Krucinska J., Wedekind J.E. A posteriori design of crystal contacts to improve the X-ray diffraction properties of a small RNA enzyme. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2007, 63:815-825.
21. Juneau K., Podell E., Harrington D.J., Cech T.R. Structural basis of the enhanced stability of a mutant ribozyme domain and a detailed view of RNA-solvent interactions. Structure 2001, 9:221-231.
22. Guo F., Cech T.R. Evolution of Tetrahymena ribozyme mutants with increased structural stability. Nat. Struct. Biol. 2002, 9:855-861.
23. Guo F., Gooding A.R., Cech T.R. Structure of the Tetrahymena ribozyme base triple sandwich and metal ion at the active site. Mol. Cell 2004, 16:351-362.
24. Vicens Q., Gooding A.R., Laederach A., Cech T.R. Local RNA structural changes induced by crystallization are revealed by SHAPE. RNA 2007, 13:536-548.
25. Liu J., Lilley D.M.J. The role of specific 2′-hydroxyl groups in the stabilization of the folded conformation of kink-turn RNA. RNA 2007, 13:200-210.
26. Garst A.D., Héroux A., Rambo R.P., Batey R.T. Crystal structure of the lysine riboswitch regulatory mRNA element. J. Biol. Chem. 2008, 283:22347-22351.
27. Serganov A., Huang L., Patel D.J. Structural insights into amino acid binding and gene control by a lysine riboswitch. Nature 2008, 455:1263-1267.
28. Goody T.A., Melcher S.E., Norman D.G., Lilley D.M.J. The kink-turn motif in RNA is dimorphic, and metal ion-dependent. RNA 2004, 10:254-264.
29. Edwards T.E., Ferre-D'Amare A.R. Crystal structures of the thi-box riboswitch bound to thiamine pyrophosphate analogs reveal adaptive RNA-small molecule recognition. Structure 2006, 14:1459-1468.
30. Gilbert S.D., Reyes F.E., Edwards A.L., Batey R.T. Adaptive ligand binding by the purine riboswitch in the recognition of guanine and adenine analogs. Structure 2009, 17:857-868.
31. Thore S., Frick C., Ban N. Structural basis of thiamine pyrophosphate analogues binding to the eukaryotic riboswitch. J. Am. Chem. Soc. 2008, 130:8116-8117.
32. Yuan Z., Zhao J., Wang Z.-X. Flexibility analysis of enzyme active sites by crystallographic temperature factors. Protein Eng. 2003, 16:109-114.
33. Parasarathy S., Murthy M.R. Analysis of temperature factor distribution in high-resolution protein structures. Protein Sci. 1997, 6:2561-2567.
34. Carugo O., Argos P. Accessibility to internal cavities and ligand binding sites monitored by protein crystallographic thermal factors. Proteins 1998, 31:201-213.
35. Theobald D.L., Wuttke D.S. THESEUS: maximum likelihood superpositioning and analysis of macromolecular structures. Bioinformatics 2006, 22:2171-2172.
36. Thomas C.B., Scavetta R.D., Gumport R.I., Churchill M.E. Structures of liganded and unliganded RsrI N6-adenine DNA methyltransferase: a distinct orientation for active cofactor binding. J. Biol. Chem. 2003, 278:26094-26101.
37. Griffith S.C., Sawaya M.R., Boutz D.R., Thapar N., Katz J.E., Clarke S., Yeates T.O. Crystal structure of a protein repair methyltransferase from Pyrococcus furiosus with its l-isoaspartyl peptide substrate. J. Mol. Biol. 2001, 313:1103-1116.
38. Shoeman R., Redfield B., Coleman T., Greene R.C., Smith A.A., Brot N., Weissbach H. Regulation of methionine synthesis in Escherichia coli: effect of metJ gene product and S-adenosylmethionine on the expression of the metF gene. Proc. Natl Acad. Sci. USA 1985, 82:3601-3605.
39. Phillips K., Phillips S.E.V. Electrostatic activation of Escherichia coli methionine repressor. Structure 1994, 2:309-316.
40. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1998, 54:905-921.
41. Zheng L., Baumann U., Reymond J. An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 2004, 32:e115.
42. Kieft J.S., Batey R.T. A general method for rapid and nondenaturing purification of RNAs. RNA 2004, 10:988-995.
43. Pflugrath J.W. The finer things in X-ray diffraction data collection. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1999, 55:1718-1725.
44. Rigaku, C. (2002). CrystalClear: an integrated program for the collection and processing of area detector data.
45. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
46. Adams P.D., Grosse-Kunstleve R.W., Hung L.W., Ioerger T.R., McCoy A.J., Moriarty N.W. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2002, 58:1948-1954.
47. Strong M., Sawaya M.R., Wang S., Phillips M., Cascio D., Eisenberg D. Toward the structural genomics of complexes: crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 2006, 103:8060-8065.
48. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60:2126-2132.
49. The Merck Index 1983, Merck & Co., Inc., Rahway, NJ. 10th edit. M. Windholz, S. Budavari, R. Blumetti, E. Otterbein (Eds.).
50. MicroCal, LLC. (2003). VP-ITC Microcalorimeter User's Manual, MicroCal, LLC, Northampton, MA.
51. Turnbull W.B., Daranas A.H. On the value of c: can low affinity systems be studied by isothermal titration calorimetry?. J. Am. Chem. Soc. 2003, 125:14859-14866.
52. Tellinghuisen J. Optimizing experimental parameters in isothermal titration calorimetry: variable volume procedures. J. Phys. Chem. B 2007, 111:11531-11537.
53. Tellinghuisen J. Isothermal titration calorimetry at very low c. Anal. Biochem. 2008, 373:395-397.
54. Wiseman T., Williston S., Brandts J.F., Lin L.N. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal. Biochem. 1989, 179:131-137.